Trachypithecus Leucocephalus Research Articles

广西扶绥黑叶猴和白头叶猴冬季主要食物水分含量的比较研究

广西扶绥黑叶猴和白头叶猴冬季主要食物水分含量的比较研究

Effect of Group Size on Time Budgets and Ranging Behavior of White-Headed Langurs in Limestone Forest, Southwest China

The ecological constraints model is well supported by data from most frugivorous primates; however, the prediction power of the model is weak for folivorous primates. From September 2016 to August 2017, we collected comparative data on time budgets, daily path lengths and diets of four groups of white-headed langurs (Trachypithecus leucocephalus), including two large groups (G-DS and G-ZWY) and two small groups (G-LZ and G-NN) in Chongzuo White-Headed Langur National Nature Reserve, Guangxi Province, Southwest China. The aim was to obtain evidence of foraging competition and to test the ecological constraints model on this highly folivorous primate in its karst habitat. The results showed that langurs in the larger groups spent more time traveling, less time resting, and had a longer average daily path length than those in the small groups. Diet composition and dietary diversity were not significantly different between the large and small groups. Our study demonstrates that langurs from large groups suffer scramble competition in limestone forests and supports the validity of the ecological constraints model for folivores.

Low genetic diversity in a critically endangered primate: shallow evolutionary history or recent population bottleneck?

BackgroundCurrent patterns of population genetic variation may have been shaped by long-term evolutionary history and contemporary demographic processes. Understanding the underlying mechanisms that yield those patterns is crucial for informed conservation of endangered species. The critically endangered white-headed langur, Trachypithecus leucocephalus, is endemic to a narrow range in southwest China. This species shows very low genetic diversity in its 2 main relict populations, Fusui and Chongzuo. Whether this has been caused by a short evolutionary history or recent population declines is unknown. Therefore, we investigated the contributions of historical and recent population demographic changes to population genetic diversity by using 15 nuclear microsatellite markers and mitochondrial DNA (mtDNA) control region sequences.ResultsUsing genetic data from 214 individuals we found a total of 9 mtDNA haplotypes in the Fusui population but only 1 haplotype in the Chongzuo population, and we found an overall low genetic diversity (haplotype and nucleotide diversities: h = 0.486 ± 0.036; π = 0.0028 ± 0.0003). The demographic history inferred from mtDNA and microsatellite markers revealed no evidence for historical population size fluctuations or recent population bottlenecks. Simulations of possible population divergence histories inferred by DIYABC analysis supported a recent divergence of the Chongzuo population from the Fusui population and no population bottlenecks.ConclusionsDespite severe population declines caused by anthropogenic activities in the last century, the low genetic diversity of the extant white-headed langur populations is most likely primarily due to the species’ shallow evolutionary history and to a recent, local population founder event.

Home Range Size and Habitat use by Cat Ba Langurs (Trachypithecus poliocephalus) in a Disturbed and Fragmented Habitat

Primate home range size and habitat use are affected by resource availability, which may change seasonally. Limestone langurs (Trachypithecus genus), including the Critically Endangered Cat Ba langur (Trachypithecus poliocephalus), live on limestone karst hills with shrubby and discontinuous vegetation. This study explores home range size and habitat use in relation to substrate, vegetation coverage, and hill type for Cat Ba langurs living on Cat Ba Island. We predicted that home range size would be similar to that of other limestone langurs and that as resources vary seasonally and across habitat types, habitat use would vary with season and behavior, with foraging concentrated on slopes, where food is plentiful. We collected 180 days of observational data on two reproductive groups (N = 7 and N = 10–13), taking GPS fixes of the group whenever they moved farther than the typical group spread to determine home ranges, and 10-min instantaneous scans to assess habitat use. The two groups had home ranges of 22 ha and 50 ha (0.32 and 0.20–0.26 individuals/ha respectively). Ranges for both groups were smaller in the dry season than the wet season, although we could not assess seasonal variation statistically. The langurs spent most scans on rocks, in sparsely vegetated areas, and on exposed slopes and steep cliffs; however they foraged primarily on gradually inclined slopes, especially in the dry season. These results suggest that conservation efforts should focus on protecting nutritionally important valleys and exposed slopes to ensure year-long access to food resources. It may, however, be difficult to balance human and nonhuman primate habitat use.

Erratum to: Seasonal Variation in the Activity and Dietary Budgets of Cat Ba Langurs (Trachypithecus poliocephalus)

Primate activity budgets are dictated by food availability and distribution; thus primates living in seasonal environments must adapt their behaviors to accommodate fluctuations in resources. Cat Ba langurs (Trachypithecus poliocephalus), a Critically Endangered Asian colobine and a member of the limestone langur group (francoisi superspecies group within genus Trachypithecus), live only in fragmented and disturbed habitats on Cat Ba Island, northeastern Vietnam. This study aimed to assess the behaviors and diet of Cat Ba langurs by group, age, sex, and season. We predicted they would have high rates of inactivity and foraging, low rates of social behaviors, with seasonal variation that reflects an energy-maximizing strategy. We conducted behavioral observations through scan sampling over an 11-month period and found that Cat Ba langurs spent a significant portion of their day inactive (57 %) followed by foraging (18 %), socializing (13 %), locomoting (10 %), and engaging in “other” behaviors (2 %). Their diet was made up primarily of leaves (83 %) followed by flowers (8 %), fruit (6 %), and stems (3 %). We found groups to differ in diet and activity, which is likely owing to differences in demographics and home range between groups. Seasonally, the animals ate more leaves and spent more time foraging in the dry season than the wet season, suggesting that they are energy maximizers. Cat Ba langurs have activity and dietary budgets similar to those of other limestone langurs, and respond to a presumed seasonal fluctuation in food availability similarly.

A White-headed langurs impulsive state feedback control model with sparse effect and continuous delay

In this paper, a white-headed langurs impulsive state feedback control model with sparse effect and continuous delay is investigated. We get the sufficient condition under which the system has a unique order-1 periodic solution through the method of successor function, and prove the stability of the order-1 periodic solution by the limit method of the successor point sequences. Furthermore, we perform numerical analysis on the theoretical results. Our results show that artificial breeding andreleasing langurs in captive tothe wild can effectively protect wild white-headed langurs with sparse effect and continuous delay.

Low genetic diversity and strong population structure shaped by anthropogenic habitat fragmentation in a critically endangered primate, Trachypithecus leucocephalus.

Habitat fragmentation may strongly impact population genetic structure and reduce the genetic diversity and viability of small and isolated populations. The white-headed langur (Trachypithecus leucocephalus) is a critically endangered primate species living in a highly fragmented and human-modified habitat in southern China. We examined the population genetic structure and genetic diversity of the species and investigated the environmental and anthropogenic factors that may have shaped its population structure. We used 214 unique multi-locus genotypes from 41 social groups across the main distribution area of T. leucocephalus, and found strong genetic structure and significant genetic differentiation among local populations. Our landscape genetic analyses using a causal modelling framework suggest that a large habitat gap and geographical distance represent the primary landscape elements shaping genetic structure, yet high levels of genetic differentiation also exist between patches separated by a small habitat gap or road. This is the first comprehensive study that has evaluated the population genetic structure and diversity of T. leucocephalus using nuclear markers. Our results indicate strong negative impacts of anthropogenic land modifications and habitat fragmentation on primate genetic connectivity between forest patches. Our analyses suggest that two management units of the species could be defined, and indicate that habitat continuity should be enforced and restored to reduce genetic isolation and enhance population viability.

Effect of habitat fragmentation on ranging behavior of white-headed langurs in limestone forests in Southwest China.

The critically endangered white-headed langur (Trachypithecus leucocephalus) is confined to fragmented karst forests of southwest Guangxi Province, China. A lack of information on the influence of habitat fragmentation on langur behavior has prevented a comprehensive understanding of their ranging behavior and the development of effective langur conservation strategies. We collected comparative data on time budgets, daily path lengths, home range and diets of four langur groups inhabiting the lightly fragmented Fusui forest (G1, G2) and the more heavily fragmented Chongzuo forest (G3, G4). The aim was to explore the effect of this fragmentation on langur ranging behavior. Our results showed that the Fusui groups spent more time on moving and less time on feeding and playing than the Chongzuo groups. Daily path lengths were 472.4-536.1m for the Fusui groups and 449.6-480.7m for the Chongzuo groups, indicating no marked inter-site variation. The Fusui groups occupied much larger home ranges (23.8-33.8ha) than the Chongzuo groups (14.5-15.8ha). However, all groups had similar monthly home ranges. Diets significantly differed among langur groups. The Fusui groups consumed more young leaves and had much lower diet diversity compared with the Chongzuo groups. Our findings indicate that habitat fragmentation is one of the crucial determinants of white-headed langur ranging behavior because fragmentation reduces and restricts the home range. Langurs in fragmented habitat adopt an energy conservation strategy characterized by devoting more time to feeding and less time to moving, with a smaller home range and consumption of more plant species. We argue that linking fragmented forests with corridors should be considered a priority in a wider and comprehensive longer term langur population conservation and habitat management strategy.

Fine-scale genetic structure analyses reveal dispersal patterns in a critically endangered primate, Trachypithecus leucocephalus.

Dispersal is a critically important life history trait of social organisms that has a major impact on the population genetic structure and social relationships within groups. Primates exhibit highly diversified dispersal and philopatry patterns, but knowledge of these patterns is difficult to obtain and usually limited to observations of a small number of focal social groups or individuals. Here, we investigated the dispersal pattern of a critically endangered colobine monkey, the white-headed langur (Trachypithecus leucocephalus), using molecular approaches, and sex-specific population genetic structure analyses at fine geographical scales. We non-invasively collected 403 fecal samples from 41 social groups across 90% of the langur's range in Fusui (FS) and Chongzuo (CZ) in southwestern Guangxi Province, China. We identified 214 unique individuals from the samples by genotyping 15 polymorphic autosomal microsatellite loci, a sex-specific marker, and sequencing the mitochondrial DNA (mtDNA) hypervariable region I (HVRI). We found higher intragroup than intergroup genetic relatedness in males and females in both populations. A significant positive correlation between genetic distance and geographical distance, that is a pattern of isolation-by-distance, was detected in females from the FS population, but not in males. Spatial autocorrelation analyses revealed high within-group relatedness in both sexes and populations, as well as an additional positive correlation at the 0.5-km distance class in females from the FS population. Furthermore, we inferred first-generation migrants using genetic assignment tests. Our results suggest that male T. leucocephalus disperse at random distances within habitat areas, whereas dispersal of females may mainly occur among adjacent groups near their home site. Our study provides the first genetic evidence for sex-biased dispersal in T. leucocephalus, which has important management and conservation implications for the species.

Complete mitochondrial genome of Trachypithecus poliocephalus (Primates: Cercopithecidae)

Trachypithecus poliocephalus : (Primates: Cercopithecidae), classified as critically endangered (IUCN) and in China was listed National First Class Protected Animal. In this study, the complete mitochondrial genome sequence of T. poliocephalus has been reported for the first time in China. The complete mitochondrial genome of T. poliocephalus was sequenced and it contained 13 protein-coding genes, 2 rRNA genes (12S rRNA and 16S rRNA), 22 tRNA genes, and one control region (D-loop).

Seasonal Variation in the Activity and Dietary Budgets of Cat Ba Langurs (Trachypithecus poliocephalus)

Seasonal Variation in the Activity and Dietary Budgets of Cat Ba Langurs (Trachypithecus poliocephalus)

Isolation of microsatellite loci and reliable genotyping using noninvasive samples of a critically endangered primate, Trachypithecus leucocephalus.

Genetic information can be critical in identifying conservation priorities and developing conservation strategies. There is an urgent need for noninvasive genetic tools to study the wild populations of Asian colobine monkeys. The majority of these species are threatened with habitat destruction, population reduction and even extinction, but generally lack information on their genetic diversity and population structure. Genetic sampling and tissue collection have been scarce in these species owing to strict regulations on manipulation of endangered species, and the difficulties and risks associated with capturing these arboreal and fast-moving monkeys in the challenging environments that they inhabit. These difficulties have hindered the development of molecular genetic markers, which are usually derived from tissues or blood. In this study, we present a method for de novo microsatellite isolation and genotyping using DNA from noninvasive origins of a critically endangered Asian colobine, the white-headed langur (Trachypithecus leucocephalus). Genomic DNA isolated from hair was shown to be sufficient for microsatellite enrichment and isolation, with similar isolation efficiencies as from tissue DNA. We identified and characterized 20 polymorphic microsatellite loci, and evaluated their amplification success and genotyping reliability with 86 field-collected fecal samples. These results show that this panel of loci can produce reliable genotypes from fecal samples, and represent a useful tool for noninvasive investigation of genetic structure, individual identification and kinship assessment in this highly endangered species. Our approach can be applied to conservation genetic studies of other wild species that lack sequence information and tissue samples.

Dietary adaptation of white-headed langurs in a fragmented limestone habitat

AbstractInformation on feeding habits and food choices of species living in heavily disturbed and fragmented habitats is critical to developing conservation plans for these animals. We collected data on the diet and food choices of two groups (Groups 1 and 2) of white-headed langurs (

An impulsive state feedback control model for releasing white-headed langurs in captive to the wild

In this paper, an impulsive state feedback control model for releasing white-headed langurs in captive to the wild is investigated. By using the geometric theory of semi-continuous dynamic system, the method of successor functions and the analogue of the Poincare criterion, it is proved that under certain conditions the system has an order-1 periodic solution with trajectory asymptotical stability, and this periodic solution remains above some critical value. The theoretical results are verified by the numerical simulations. The conclusion is that simultaneously taking the measures of both population migration and artificial breeding can effectively protect wild white-headed langurs, so that the population can continue to survive and can avoid becoming extinct.

Low Genetic Diversity and Strong Geographical Structure of the Critically Endangered White-Headed Langur (Trachypithecus leucocephalus) Inferred from Mitochondrial DNA Control Region Sequences.

Many Asian colobine monkey species are suffering from habitat destruction and population size decline. There is a great need to understand their genetic diversity, population structure and demographic history for effective species conservation. The white-headed langur (Trachypithecus leucocephalus) is a Critically Endangered colobine species endemic to the limestone karst forests in southwestern China. We analyzed the mitochondrial DNA (mtDNA) control region sequences of 390 fecal samples from 40 social groups across the main distribution areas, which represented one-third of the total extant population. Only nine haplotypes and 10 polymorphic sites were identified, indicating remarkably low genetic diversity in the species. Using a subset of 77 samples from different individuals, we evaluated genetic variation, population structure, and population demographic history. We found very low values of haplotype diversity (h = 0.570 ± 0.056) and nucleotide diversity (π = 0.00323 ± 0.00044) in the hypervariable region I (HVRI) of the mtDNA control region. Distribution of haplotypes displayed marked geographical pattern, with one population (Chongzuo, CZ) showing a complete lack of genetic diversity (having only one haplotype), whereas the other population (Fusui, FS) having all nine haplotypes. We detected strong population genetic structure among habit patches (Φ ST = 0.375, P < 0.001). In addition, the Mantel test showed a significant correlation between the pairwise genetic distances and geographical distances among social groups in FS (correlation coefficient = 0.267, P = 0.003), indicting isolation-by-distance pattern of genetic divergence in the mtDNA sequences. Analyses of demographic history suggested an overall stable historical population size and modest population expansion in the last 2,000 years. Our results indicate different genetic diversity and possibly distinct population history for different local populations, and suggest that CZ and FS should be considered as one evolutionarily significant unit (ESU) and two management units (MUs) pending further investigation using nuclear markers.

Aspidistra chongzuoensis (Asparagaceae): a new species from limestone areas in Guangxi, China

During our fieldwork in the southwest Guangxi, China in January 2014, we found in the White-headed Langur National Nature Reserve an unusual Aspidistra Ker-Gawler (1822: 628) specimen with fruits and dried up flowers only, so we could not identify it without fresh flowers. In November, we returned to the place for further observations of the species, and found the plants with blackish purple, bell-shaped flowers. After consulting herbarium specimens and relevant literature on Aspidistra (Liang &amp; Tamura 2000, Li 2004, Li &amp; Wei 2003, Tillich 2005, 2008, Lin et al. 2009, 2010, 2012, 2013, Lin &amp; Liu 2011, Liu et al. 2011, Tillich &amp; Leong-Skornickova 2013, Hu et al. 2014, Meng et al. 2014, Vislobokov et al. 2014), it became apparent that this population is an undescribed species, and the valid name Aspidistra chongzuoensis was used, which is described below.

Nonmaternal Infant Handling in Wild White-Headed Langurs (Trachypithecus leucocephalus)

Infants of many primate species have extensive interactions with group members other than their mothers, which can affect an infant’s fitness. Patterns of nonmaternal infant handling vary according to the mother’s response as well as the number, sex, age, and dominance ranks of social partners. The primary goal of this study was to identify the basic pattern and explore the function of nonmaternal infant handling behavior in wild white-headed langurs (Trachypithecus leucocephalus) at the Nongguan Hills in Guangxi, Southwest China. We report nonmaternal interactions in the first 3 mo after birth for 15 infants born during six birth seasons in a 67-mo field study. The nonmaternal infant handling we observed was generally in the form of caregiving, and mothers permitted most handling attempts. Infants were handled by nonmothers from the first day after birth. Infants spent 20–30% of the daytime associated with nonmothers during the first month of life, and time in contact with nonmothers decreased with infant age. Rates of nonmaternal infant handling varied significantly with the sex and age of handlers. Juvenile and subadult females handled infants significantly more than expected from their proportional representations in the group, whereas adult females did so less frequently than expected. Older male infants and juvenile males rarely handled infants, and adult males never did so. Infant handling behavior showed no correlation with the dominance rank of handlers relative to the mothers. Our data, although limited in some analyses, are in line with the predictions of the learning-to-mother hypothesis, but do not support the female competition or alliance formation hypotheses.

Multilocus typing of Cryptosporidium spp. and Giardia duodenalis from non-human primates in China

Non-human primates (NHPs) are commonly infected with Cryptosporidium spp. and Giardia duodenalis. However, molecular characterisation of these pathogens from NHPs remains scarce. In this study, 2,660 specimens from 26 NHP species in China were examined and characterised by PCR amplification of 18S rRNA, 70kDa heat shock protein (hsp70) and 60kDa glycoprotein (gp60) gene loci for Cryptosporidium; and 1,386 of the specimens by ssrRNA, triosephosphate isomerase (tpi) and glutamate dehydrogenase (gdh) gene loci for Giardia. Cryptosporidium was detected in 0.7% (19/2660) specimens of four NHP species including rhesus macaques (0.7%), cynomolgus monkeys (1.0%), slow lorises (10.0%) and Francois’ leaf monkeys (6.7%), belonging to Cryptosporidium hominis (14/19) and Cryptosporidium muris (5/19). Two C. hominis gp60 subtypes, IbA12G3 and IiA17 were observed. Based on the tpi locus, G. duodenalis was identified in 2.2% (30/1,386) of specimens including 2.1% in rhesus macaques, 33.3% in Japanese macaques, 16.7% in Assam macaques, 0.7% in white-headed langurs, 1.6% in cynomolgus monkeys and 16.7% in olive baboons. Sequence analysis of the three targets indicated that all of the Giardia-positive specimens belonged to the zoonotic assemblage B. Highest sequence polymorphism was observed at the tpi locus, including 11 subtypes: three known and eight new ones. Phylogenetic analysis of the subtypes showed that most of them were close to the so-called subtype BIV. Intragenotypic variations at the gdh locus revealed six types of sequences (three known and three new), all of which belonged to so-called subtype BIV. Three specimens had co-infection with C. hominis (IbA12G3) and G. duodenalis (BIV). The presence of zoonotic genotypes and subtypes of Cryptosporidium spp. and G. duodenalis in NHPs suggests that these animals can potentially contribute to the transmission of human cryptosporidiosis and giardiasis.

Birth intervention and non-maternal infant-handling during parturition in a nonhuman primate.

Direct intervention in infant delivery by non-parturient individuals is a rare phenomenon in nonhuman primates. In contrast, birth assistance by other individuals, or the practice of midwifery, is universal among human societies and generally believed to be a behavior unique to our species. It has been proposed that the enlarged head of the human fetus and the relatively narrow birth canal constrained by bipedalism has made human parturition more difficult than in nonhuman primates, and these anatomic challenges have led to the rotation of the fetus in the birth canal and an occiput anterior (i.e., backward-facing) orientation of emergence. These characteristics have hindered the mother's ability to self-assist the delivery of the infant, therefore necessitating assistance by other individuals or midwives for successful birth. Here we report the first high-definition video recordings of birth intervention behavior in a wild nonhuman primate, the white-headed langur (Trachypithecus leucocephalus). We observed that while a primiparous female gave birth to an infant in an occiput posterior (i.e., forward-facing) orientation, a multiparous female intervened in the delivery by manually pulling the infant out of the birth canal and cared for it in the following hours. Our finding shows extensive social interactions throughout parturition, and presents an unequivocal case of non-maternal intervention with infant birth in a nonhuman primate.

Genetic Polymorphism and Zoonotic Potential of Enterocytozoon bieneusi from Nonhuman Primates in China

Enterocytozoon bieneusi is an important zoonotic pathogen. To assess the human-infective potential of E. bieneusi in nonhuman primates (NHPs), we examined the prevalence and genotype distribution of E. bieneusi in 23 NHP species by PCR and sequence analysis of the ribosomal internal transcribed spacer (ITS). A total of 1,386 fecal specimens from NHPs from five provinces in China were examined, and E. bieneusi was detected in 158 (11.4%) specimens from five NHP species, including cynomolgus monkey (67.7%), rhesus macaque (8.8%), Japanese macaque (33.3%), white-headed langur (13.6%), and golden snub-nosed monkey (3.5%) (P < 0.0001). The infection rates were 70.2%, 21.5%, 8.5%, 7.5%, and 5.6% in Guangdong, Yunnan, Guangxi, Henan, and Sichuan Provinces, respectively (P < 0.0001). The prevalence was significantly higher in captive (13.7%) than in free-range (5.0%) animals (P < 0.0001). Altogether, 16 ITS genotypes were observed, including nine known genotypes (IV, D, Henan V, Peru8, PigEBITS7, EbpC, Peru11, BEB6, and I) and seven new genotypes (CM1 to CM7). The common genotypes included CM1, IV, and D, which were detected in 43, 31, and 30 specimens, respectively. Phylogenetic analysis revealed that seven known genotypes (but not BEB6 and I) and four new genotypes (CM1, CM2, CM3, and CM6) belonged to the previously described group 1 with zoonotic potential. Genotypes CM5 and CM7 clustered with group 2, whereas genotype CM4 did not belong to any of the previously proposed groups. It was concluded that humans and NHPs residing in the same geographical location shared the same E. bieneusi genotypes, indicating a potential role of these animals in the zoonotic transmission of E. bieneusi.